Secretory phospholipases A2 are secreted from ciliated cells and increase mucin and eicosanoid secretion from goblet cells

Chest

Volumn 147, Issue 6, 2015, Pages 1599-1609

  Tanabe, Tsuyoshi ^a   Shimokawaji, Tadasuke ^a   Kanoh, Soichiro ^a   Rubin, Bruce K ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ICOSANOID; INTERLEUKIN 13; LEUKOTRIENE; LIPOXYGENASE; MESSENGER RNA; MUCIN; MUCIN 5AC; PHOSPHOLIPASE A2; PROSTAGLANDIN SYNTHASE; RNA; INTERLEUKIN 8; PROSTAGLANDIN E2;

ARTICLE; CELL COUNT; CELL DIFFERENTIATION; CELL GROWTH; CELL STRUCTURE; CELL SURFACE; CILIATED EPITHELIUM CELL; EPITHELIUM CELL; GOBLET CELL; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTEIN SYNTHESIS; BRONCHUS; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; EUKARYOTIC FLAGELLUM; METABOLISM; PARACRINE SIGNALING; PHYSIOLOGY;

BRONCHI; CELL DIFFERENTIATION; CELLS, CULTURED; CILIA; DINOPROSTONE; EICOSANOIDS; EPITHELIAL CELLS; GOBLET CELLS; HUMANS; INTERLEUKIN-13; INTERLEUKIN-8; LEUKOTRIENES; MUCINS; PARACRINE COMMUNICATION; PHOSPHOLIPASES A2;

EID: 84930889633     PISSN: 00123692     EISSN: 19313543     Source Type: Journal    
DOI: 10.1378/chest.14-0258     Document Type: Article

References (57)

1. Dennis EA. Phospholipase A2 in eicosanoid generation. Am J Respir Crit Care Med. 2000;161(2 pt 2):S32-S35.
2. Murakami M, Lambeau G. Emerging roles of secreted phospholipase A(2) enzymes: an update. Biochimie. 2013; 95(1):43-50.
3. Lambeau G, Gelb MH. Biochemistry and physiology of mammalian secreted phospholipases A2. Annu Rev Biochem. 2008;77:495-520.
4. Misso NL, Petrovic N, Grove C, Celenza A, Brooks-Wildhaber J, Thompson PJ. Plasma phospholipase A2 activity in patients with asthma: association with body mass index and cholesterol concentration. Thorax. 2008;63(1):21-26.
5. Kim DK, Fukuda T, Thompson BT, Cockrill B, Hales C, Bonventre JV. Bronchoalveolar lavage fluid phospholipase A2 activities are increased in human adult respiratory distress syndrome. Am J Physiol. 1995;269(1 pt 1):L109-L118.
6. Masuda S, Murakami M, Mitsuishi M, et al . Expression of secretory phospholipase A2 enzymes in lungs of humans with pneumonia and their potential prostaglandin-synthetic function in human lung-derived cells. Biochem J. 2005;387(pt 1):27-38.
7. 2 groups IIA and X in the airways and asthma severity . Clin Exp Allergy. 2011; 41 (6): 801-810.
8. Henderson WR Jr, Chi EY, Bollinger JG, et al . Importance of group X-secreted phospholipase A2 in allergen-induced airway inflammation and remodeling in a mouse asthma model. J Exp Med. 2007;204(4):865-877.
9. Muñoz NM, Meliton AY, Arm JP, Bonventre JV, Cho W, Leff AR. Deletion of secretory group V phospholipase A2 attenuates cell migration and airway hyperresponsiveness in immunosensitized mice. J Immunol. 2007;179(7):4800-4807.
10. Shoseyov D, Bibi H, Offer S, et al . Treatment of ovalbumin-induced experimental allergic bronchitis in rats by inhaled inhibitor of secretory phospholipase A(2). Thorax. 2005;60(9):747-753.
11. Okamoto K, Kim JS, Rubin BK. Secretory phospholipases A2 stimulate mucus secretion, induce airway inflammation, and produce secretory hyperresponsiveness to neutrophil elastase in ferret trachea. Am J Physiol Lung Cell Mol Physiol. 2007;292(1):L62-L67.
12. Tanabe T, Kanoh S, Tsushima K, Yamazaki Y, Kubo K, Rubin BK. Clarithromycin inhibits interleukin- 13-induced goblet cell hyperplasia in human airway cells. Am J Respir Cell Mol Biol. 2011;45(5):1075-1083.
13. Ordoñez CL, Khashayar R, Wong HH, et al. Mild and moderate asthma is associated with airway goblet cell hyperplasia and abnormalities in mucin gene expression. Am J Respir Crit Care Med. 2001;163(2):517-523.
14. Wills-Karp M, Luyimbazi J, Xu X, et al. Interleukin-13: central mediator of allergic asthma. Science. 1998;282(5397):2258-2261.
15. Atherton HC, Jones G, Danahay H. IL-13-induced changes in the goblet cell density of human bronchial epithelial cell cultures: MAP kinase and phosphatidylinositol 3-kinase regulation. Am J Physiol Lung Cell Mol Physiol. 2003;285(3):L730-L739.
16. Young HW, Williams OW, Chandra D, et al. Central role of Muc5ac expression in mucous metaplasia and its regulation by conserved 5' elements. Am J Respir Cell Mol Biol. 2007;37(3):273-290.
17. Buisine MP, Devisme L, Copin MC, et al. Developmental mucin gene expression in the human respiratory tract. Am J Respir Cell Mol Biol. 1999;20(2):209-218.
18. Evans CM, Kim K, Tuvim MJ, Dickey BF. Mucus hypersecretion in asthma: causes and effects. Curr Opin Pulm Med. 2009;15(1):4-11.
19. Triggiani M, Granata F, Giannattasio G, Marone G. Secretory phospholipases A2 in inflammatory and allergic diseases: not just enzymes. J Allergy Clin Immunol. 2005;116(5):1000-1006.
20. Lindbom J, Ljungman AG, Lindahl M, Tagesson C. Expression of members of the phospholipase A2 family of enzymes in human nasal mucosa. Eur Respir J. 2001;18(1):130-138.
21. Lindbom J, Ljungman AG, Lindahl M, Tagesson C. Increased gene expression of novel cytosolic and secretory phospholipase A(2) types in human airway epithelial cells induced by tumor necrosis factor-alpha and IFN-gamma. J Interferon Cytokine Res. 2002;22(9):947-955.
22. Seeds MC, Jones KA, Duncan Hite R, et al. Cell-specific expression of group X and group V secretory phospholipases A(2) in human lung airway epithelial cells. Am J Respir Cell Mol Biol. 2000;23(1):37-44.
23. Kanoh S, Tanabe T, Rubin BK. IL-13- induced MUC5AC production and goblet cell differentiation is steroid resistant in human airway cells. Clin Exp Allergy . 2011;41(12):1747-1756.
24. Kanoh S, Tanabe T, Rubin BK. Dapsone inhibits IL-8 secretion from human bronchial epithelial cells stimulated with lipopolysaccharide and resolves airway inflammation in the ferret. Chest. 2011;140(4):980-990.
25. Tanabe T, Kanoh S, Moskowitz WB, Rubin BK. Cardiac asthma: transforming growth factor-β from the failing heart leads to squamous metaplasia in human airway cells and in the murine lung. Chest. 2012;142(5):1274-1283.
26. Bernacki SH, Nelson AL, Abdullah L, et al. Mucin gene expression during differentiation of human airway epithelia in vitro. Muc4 and muc5b are strongly induced. Am J Respir Cell Mol Biol. 1999;20(4):595-604.
27. Thavagnanam S, Parker JC, McBrien ME, Skibinski G, Heaney LG, Shields MD. Effects of IL-13 on mucociliary differentiation of pediatric asthmatic bronchial epithelial cells. Pediatr Res. 2011;69(2):95-100.
28. Parker J, Sarlang S, Thavagnanam S, et al . A 3-D well-differentiated model of pediatric bronchial epithelium demonstrates unstimulated morphological differences between asthmatic and nonasthmatic cells. Pediatr Res. 2010;67(1): 17-22.
29. Tanabe T, Fujimoto K, Yasuo M, et al. Modulation of mucus production by interleukin-13 receptor alpha2 in the human airway epithelium. Clin Exp Allergy. 2008;38(1):122-134.
30. Tanabe T, Shimokawaji T, Kanoh S, Rubin BK. IL-33 stimulates CXCL8/IL-8 secretion in goblet cells but not normally differentiated airway cells. Clin Exp Allergy. 2014;44(4):540-552.
31. Hay DW, Torphy TJ, Undem BJ. Cysteinyl leukotrienes in asthma: old mediators up to new tricks. Trends Pharmacol Sci. 1995;16(9):304-309.
32. Jame AJ, Lackie PM, Cazaly AM, et al. Human bronchial epithelial cells express an active and inducible biosynthetic pathway for leukotrienes B4 and C4. Clin Exp Allergy. 2007;37(6):880-892.
33. Hunter JA, Finkbeiner WE, Nadel JA, Goetzl EJ, Holtzman MJ. Predominant generation of 15-lipoxygenase metabolites of arachidonic acid by epithelial cells from human trachea. Proc Natl Acad Sci U S A. 1985;82(14):4633-4637.
34. Kowalski ML, Pawliczak R, Wozniak J, et al. Differential metabolism of arachidonic acid in nasal polyp epithelial cells cultured from aspirin-sensitive and aspirin-tolerant patients. Am J Respir Crit Care Med. 2000;161(2 pt 1):391-398.
35. Alcorn JF, Crowe CR, Kolls JK. TH17 cells in asthma and COPD. Annu Rev Physiol. 2010;72:495-516.
36. Sidebotham HJ, Roche WR. Asthma deaths; persistent and preventable mortality. Histopathology. 2003;43(2):105-117.
37. Kuyper LM, Paré PD, Hogg JC, et al. Characterization of airway plugging in fatal asthma. Am J Med. 2003;115(1):6-11.
38. Murakami M, Taketomi Y, Sato H, Yamamoto K. Secreted phospholipase A2 revisited. J Biochem. 2011;150(3):233-255.
39. Bezzine S, Koduri RS, Valentin E, et al. Exogenously added human group X secreted phospholipase A(2) but not the group IB, IIA, and V enzymes efficiently release arachidonic acid from adherent mammalian cells. J Biol Chem. 2000;275(5):3179-3191.
40. Murakami M, Shimbara S, Kambe T, et al. The functions of five distinct mammalian phospholipase A2S in regulating arachidonic acid release. Type IIa and type V secretory phospholipase A2S are functionally redundant and act in concert with cytosolic phospholipase A2. J Biol Chem. 1998;273(23):14411-14423.
41. Murakami M, Kambe T, Shimbara S, et al. Different functional aspects of the group II subfamily (Types IIA and V) and type X secretory phospholipase A(2)s in regulating arachidonic acid release and prostaglandin generation. Implications of cyclooxygenase-2 induction and phospholipid scramblase-mediated cellular membrane perturbation. J Biol Chem. 1999;274(44):31435-31444.
42. Murakami M, Koduri RS, Enomoto A, et al. Distinct arachidonate-releasing functions of mammalian secreted phospholipase A2s in human embryonic kidney 293 and rat mastocytoma RBL-2H3 cells through heparan sulfate shuttling and external plasma membrane mechanisms. J Biol Chem. 2001;276(13):10083-10096.
43. Murakami M, Masuda S, Shimbara S, et al. Cellular arachidonate-releasing function of novel classes of secretory phospholipase A2s (groups III and XII). J Biol Chem. 2003;278(12):10657-10667.
44. Marom Z, Shelhamer JH, Kaliner M. Effects of arachidonic acid, monohydroxyeicosatetraenoic acid and prostaglandins on the release of mucous glycoproteins from human airways in vitro. J Clin Invest. 1981;67(6):1695-1702.
45. Johnson HG, Chinn RA, Morton DR, McNee ML, Miller MD, Nadel JA. Diphenhydramine blocks the leukotriene-C4 enhanced mucus secretion in canine trachea in vivo. Agents Actions. 1983; 13(1):1-4.
46. Suzuki S, Takeuchi K, Ishinaga H, Basbaum C, Majima Y. Leukotriene D4 upregulates MUC2 gene transcription in human epithelial cells. Pharmacology. 2008;81(3):221-228.
47. Bai CH, Song SY, Kim YD. The inhibitory effect of the leukotriene receptor antagonist on leukotriene D4-induced MUC2/5AC gene expression and mucin secretion in human airway epithelial cells. Auris Nasus Larynx. 2007;34(2):203-206.
48. Rich B, Peatfield AC, Williams IP, Richardson PS. Effects of prostaglandins E1, E2, and F2 alpha on mucin secretion from human bronchi in vitro. Thorax. 1984;39(6):420-423.
49. Takahashi S, Takeuchi K, Okabe S. EP4 receptor mediation of prostaglandin E2-stimulated mucus secretion by rabbit gastric epithelial cells. Biochem Pharmacol. 1999;58(12):1997-2002.
50. Yagi T, Miyawaki Y, Nishikawa A, Horiyama S, Yamauchi K, Kuwano S. Prostaglandin E2-mediated stimulation of mucus synthesis and secretion by rhein anthrone, the active metabolite of sennosides A and B, in the mouse colon. J Pharm Pharmacol. 1990;42(8):542-545.
51. Muchekehu RW, Quinton PM. A new role for bicarbonate secretion in cervico-uterine mucus release. J Physiol. 2010;588(pt 13):2329-2342.
52. Sastre B, del Pozo V. Role of PGE2 in asthma and nonasthmatic eosinophilic bronchitis [published online ahead of print March 19, 2012]. Mediators Inflamm. doi:10.1155/2012/645383.
53. Pavord ID, Tattersfield AE. Bronchoprotective role for endogenous prostaglandin E2. Lancet. 1995;345(8947):436-438.
54. Gauvreau GM, Watson RM, O'Byrne PM. Protective effects of inhaled PGE2 on allergen-induced airway responses and airway inflammation. Am J Respir Crit Care Med. 1999;159(1):31-36.
55. Trudeau J, Hu H, Chibana K, Chu HW, Westcott JY, Wenzel SE. Selective down-regulation of prostaglandin E2-related pathways by the Th2 cytokine IL-13. J Allergy Clin Immunol. 2006;117(6): 1446-1454.
56. Aggarwal S, Moodley YP, Thompson PJ, Misso NL. Prostaglandin E2 and cysteinyl leukotriene concentrations in sputum: association with asthma severity and eosinophilic inflammation. Clin Exp Allergy. 2010;40(1):85-93.
57. Skibinski G, Elborn JS, Ennis M. Bronchial epithelial cell growth regulation in fibroblast cocultures: the role of hepatocyte growth factor. Am J Physiol Lung Cell Mol Physiol. 2007;293(1):L69-L76.